SHOU4 Proteins Regulate Trafficking of Cellulose Synthase Complexes to the Plasma Membrane

Joanna K. Polko, William J. Barnes, Cătălin Voiniciuc, Stephanie Doctor, Blaire Steinwand, Joseph L. Hill, Ming Tien, Markus Pauly, Charles T. Anderson, Joseph J. Kieber

Research output: Contribution to journalArticle

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Abstract

Cell walls play critical roles in plants, regulating tissue mechanics, defining the extent and orientation of cell expansion, and providing a physical barrier against pathogen attack [1]. Cellulose microfibrils, which are synthesized by plasma membrane-localized cellulose synthase (CESA) complexes, are the primary load-bearing elements of plant cell walls [2]. Cell walls are dynamic structures that are regulated in part by cell wall integrity (CWI)-monitoring systems that feed back to modulate wall properties and the synthesis of new wall components [3]. Several receptor-like kinases have been implicated as sensors of CWI [3–5], including the FEI1/FEI2 receptor-like kinases [4]. Here, we characterize two genes encoding novel plant-specific plasma membrane proteins (SHOU4 and SHOU4L) that were identified in a suppressor screen of the cellulose-deficient fei1 fei2 mutant. shou4 shou4l double mutants display phenotypes consistent with elevated levels of cellulose, and elevated levels of non-crystalline cellulose are present in this mutant. Disruption of SHOU4 and SHOU4L increases the abundance of CESA proteins at the plasma membrane as a result of enhanced exocytosis. The SHOU4/4L N-terminal cytosolic domains directly interact with CESAs. Our results suggest that the SHOU4 proteins regulate cellulose synthesis in plants by influencing the trafficking of CESA complexes to the cell surface. The regulation of the intracellular trafficking of cellulose synthase (CESAs) complexes plays a crucial role in modulating the level of cellulose synthesis in plants. Polko et al. identify two paralogous novel plasma-membrane-localized proteins that negatively regulate cellulose synthesis by inhibiting the exocytosis of CESAs.

Original languageEnglish (US)
Pages (from-to)3174-3182.e6
JournalCurrent Biology
Volume28
Issue number19
DOIs
StatePublished - Oct 8 2018

Fingerprint

cellulose synthase
protein transport
Protein Transport
Cell membranes
Cellulose
cellulose
plasma membrane
Cell Membrane
Cell Wall
cell walls
Proteins
synthesis
exocytosis
Cells
Exocytosis
membrane proteins
mutants
blood proteins
Membrane Proteins
phosphotransferases (kinases)

All Science Journal Classification (ASJC) codes

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Polko, J. K., Barnes, W. J., Voiniciuc, C., Doctor, S., Steinwand, B., Hill, J. L., ... Kieber, J. J. (2018). SHOU4 Proteins Regulate Trafficking of Cellulose Synthase Complexes to the Plasma Membrane. Current Biology, 28(19), 3174-3182.e6. https://doi.org/10.1016/j.cub.2018.07.076
Polko, Joanna K. ; Barnes, William J. ; Voiniciuc, Cătălin ; Doctor, Stephanie ; Steinwand, Blaire ; Hill, Joseph L. ; Tien, Ming ; Pauly, Markus ; Anderson, Charles T. ; Kieber, Joseph J. / SHOU4 Proteins Regulate Trafficking of Cellulose Synthase Complexes to the Plasma Membrane. In: Current Biology. 2018 ; Vol. 28, No. 19. pp. 3174-3182.e6.
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Polko, JK, Barnes, WJ, Voiniciuc, C, Doctor, S, Steinwand, B, Hill, JL, Tien, M, Pauly, M, Anderson, CT & Kieber, JJ 2018, 'SHOU4 Proteins Regulate Trafficking of Cellulose Synthase Complexes to the Plasma Membrane', Current Biology, vol. 28, no. 19, pp. 3174-3182.e6. https://doi.org/10.1016/j.cub.2018.07.076

SHOU4 Proteins Regulate Trafficking of Cellulose Synthase Complexes to the Plasma Membrane. / Polko, Joanna K.; Barnes, William J.; Voiniciuc, Cătălin; Doctor, Stephanie; Steinwand, Blaire; Hill, Joseph L.; Tien, Ming; Pauly, Markus; Anderson, Charles T.; Kieber, Joseph J.

In: Current Biology, Vol. 28, No. 19, 08.10.2018, p. 3174-3182.e6.

Research output: Contribution to journalArticle

TY - JOUR

T1 - SHOU4 Proteins Regulate Trafficking of Cellulose Synthase Complexes to the Plasma Membrane

AU - Polko, Joanna K.

AU - Barnes, William J.

AU - Voiniciuc, Cătălin

AU - Doctor, Stephanie

AU - Steinwand, Blaire

AU - Hill, Joseph L.

AU - Tien, Ming

AU - Pauly, Markus

AU - Anderson, Charles T.

AU - Kieber, Joseph J.

PY - 2018/10/8

Y1 - 2018/10/8

N2 - Cell walls play critical roles in plants, regulating tissue mechanics, defining the extent and orientation of cell expansion, and providing a physical barrier against pathogen attack [1]. Cellulose microfibrils, which are synthesized by plasma membrane-localized cellulose synthase (CESA) complexes, are the primary load-bearing elements of plant cell walls [2]. Cell walls are dynamic structures that are regulated in part by cell wall integrity (CWI)-monitoring systems that feed back to modulate wall properties and the synthesis of new wall components [3]. Several receptor-like kinases have been implicated as sensors of CWI [3–5], including the FEI1/FEI2 receptor-like kinases [4]. Here, we characterize two genes encoding novel plant-specific plasma membrane proteins (SHOU4 and SHOU4L) that were identified in a suppressor screen of the cellulose-deficient fei1 fei2 mutant. shou4 shou4l double mutants display phenotypes consistent with elevated levels of cellulose, and elevated levels of non-crystalline cellulose are present in this mutant. Disruption of SHOU4 and SHOU4L increases the abundance of CESA proteins at the plasma membrane as a result of enhanced exocytosis. The SHOU4/4L N-terminal cytosolic domains directly interact with CESAs. Our results suggest that the SHOU4 proteins regulate cellulose synthesis in plants by influencing the trafficking of CESA complexes to the cell surface. The regulation of the intracellular trafficking of cellulose synthase (CESAs) complexes plays a crucial role in modulating the level of cellulose synthesis in plants. Polko et al. identify two paralogous novel plasma-membrane-localized proteins that negatively regulate cellulose synthesis by inhibiting the exocytosis of CESAs.

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Polko JK, Barnes WJ, Voiniciuc C, Doctor S, Steinwand B, Hill JL et al. SHOU4 Proteins Regulate Trafficking of Cellulose Synthase Complexes to the Plasma Membrane. Current Biology. 2018 Oct 8;28(19):3174-3182.e6. https://doi.org/10.1016/j.cub.2018.07.076